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. 1997 Aug;73(2):1110–1117. doi: 10.1016/S0006-3495(97)78143-8

High-gain, low-noise amplification in olfactory transduction.

S J Kleene 1
PMCID: PMC1181007  PMID: 9251827

Abstract

It is desirable that sensory systems use high-gain, low-noise amplification to convert weak stimuli into detectable signals. Here it is shown that a pair of receptor currents underlying vertebrate olfactory transduction constitutes such a scheme. The primary receptor current is an influx of Na+ and Ca2+ through cAMP-gated channels in the olfactory cilia. External divalent cations improve the signal-to-noise properties of this current, reducing the mean current and the current variance. As Ca2+ enters the cilium, it gates Cl- channels, activating a secondary depolarizing receptor current. This current amplifies the primary current, but introduces little additional noise. The system of two currents plus divalent cations in the mucus produces a large receptor current with very low noise.

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Selected References

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  1. Boekhoff I., Tareilus E., Strotmann J., Breer H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 1990 Aug;9(8):2453–2458. doi: 10.1002/j.1460-2075.1990.tb07422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. doi: 10.1016/0092-8674(91)90418-x. [DOI] [PubMed] [Google Scholar]
  3. Firestein S., Shepherd G. M. Interaction of anionic and cationic currents leads to a voltage dependence in the odor response of olfactory receptor neurons. J Neurophysiol. 1995 Feb;73(2):562–567. doi: 10.1152/jn.1995.73.2.562. [DOI] [PubMed] [Google Scholar]
  4. Firestein S., Shepherd G. M., Werblin F. S. Time course of the membrane current underlying sensory transduction in salamander olfactory receptor neurones. J Physiol. 1990 Nov;430:135–158. doi: 10.1113/jphysiol.1990.sp018286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Frings S., Lynch J. W., Lindemann B. Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J Gen Physiol. 1992 Jul;100(1):45–67. doi: 10.1085/jgp.100.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Frings S., Seifert R., Godde M., Kaupp U. B. Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron. 1995 Jul;15(1):169–179. doi: 10.1016/0896-6273(95)90074-8. [DOI] [PubMed] [Google Scholar]
  7. Joshi H., Getchell M. L., Zielinski B., Getchell T. V. Spectrophotometric determination of cation concentrations in olfactory mucus. Neurosci Lett. 1987 Dec 4;82(3):321–326. doi: 10.1016/0304-3940(87)90276-x. [DOI] [PubMed] [Google Scholar]
  8. Kleene S. J. Basal conductance of frog olfactory cilia. Pflugers Arch. 1992 Jul;421(4):374–380. doi: 10.1007/BF00374226. [DOI] [PubMed] [Google Scholar]
  9. Kleene S. J. Block by external calcium and magnesium of the cyclic-nucleotide-activated current in olfactory cilia. Neuroscience. 1995 Jun;66(4):1001–1008. doi: 10.1016/0306-4522(94)00634-h. [DOI] [PubMed] [Google Scholar]
  10. Kleene S. J., Cejtin H. C. Solving buffering problems with Mathematica software. Anal Biochem. 1994 Nov 1;222(2):310–314. doi: 10.1006/abio.1994.1497. [DOI] [PubMed] [Google Scholar]
  11. Kleene S. J., Gesteland R. C., Bryant S. H. An electrophysiological survey of frog olfactory cilia. J Exp Biol. 1994 Oct;195:307–328. doi: 10.1242/jeb.195.1.307. [DOI] [PubMed] [Google Scholar]
  12. Kleene S. J., Gesteland R. C. Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci. 1991 Nov;11(11):3624–3629. doi: 10.1523/JNEUROSCI.11-11-03624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kleene S. J. Origin of the chloride current in olfactory transduction. Neuron. 1993 Jul;11(1):123–132. doi: 10.1016/0896-6273(93)90276-w. [DOI] [PubMed] [Google Scholar]
  14. Kleene S. J., Pun R. Y. Persistence of the olfactory receptor current in a wide variety of extracellular environments. J Neurophysiol. 1996 Apr;75(4):1386–1391. doi: 10.1152/jn.1996.75.4.1386. [DOI] [PubMed] [Google Scholar]
  15. Kleene S. J. The cyclic nucleotide-activated conductance in olfactory cilia: effects of cytoplasmic Mg2+ and Ca2+. J Membr Biol. 1993 Feb;131(3):237–243. doi: 10.1007/BF02260112. [DOI] [PubMed] [Google Scholar]
  16. Kurahashi T. Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt. J Physiol. 1989 Dec;419:177–192. doi: 10.1113/jphysiol.1989.sp017868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kurahashi T., Kaneko A. Gating properties of the cAMP-gated channel in toad olfactory receptor cells. J Physiol. 1993 Jul;466:287–302. [PMC free article] [PubMed] [Google Scholar]
  18. Kurahashi T., Yau K. W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature. 1993 May 6;363(6424):71–74. doi: 10.1038/363071a0. [DOI] [PubMed] [Google Scholar]
  19. Larsson H. P., Kleene S. J., Lecar H. Noise analysis of ion channels in non-space-clamped cables: estimates of channel parameters in olfactory cilia. Biophys J. 1997 Mar;72(3):1193–1203. doi: 10.1016/S0006-3495(97)78767-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lowe G., Gold G. H. Nonlinear amplification by calcium-dependent chloride channels in olfactory receptor cells. Nature. 1993 Nov 18;366(6452):283–286. doi: 10.1038/366283a0. [DOI] [PubMed] [Google Scholar]
  21. Lowe G., Gold G. H. Olfactory transduction is intrinsically noisy. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7864–7868. doi: 10.1073/pnas.92.17.7864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lowe G., Gold G. H. The spatial distributions of odorant sensitivity and odorant-induced currents in salamander olfactory receptor cells. J Physiol. 1991 Oct;442:147–168. doi: 10.1113/jphysiol.1991.sp018787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lowe G., Nakamura T., Gold G. H. Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5641–5645. doi: 10.1073/pnas.86.14.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
  25. Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 1985 Jul 18;316(6025):255–258. doi: 10.1038/316255a0. [DOI] [PubMed] [Google Scholar]
  26. Picones A., Korenbrot J. I. Spontaneous, ligand-independent activity of the cGMP-gated ion channels in cone photoreceptors of fish. J Physiol. 1995 Jun 15;485(Pt 3):699–714. doi: 10.1113/jphysiol.1995.sp020763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shirley S. G., Robinson C. J., Dickinson K., Aujla R., Dodd G. H. Olfactory adenylate cyclase of the rat. Stimulation by odorants and inhibition by Ca2+. Biochem J. 1986 Dec 1;240(2):605–607. doi: 10.1042/bj2400605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sklar P. B., Anholt R. R., Snyder S. H. The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J Biol Chem. 1986 Nov 25;261(33):15538–15543. [PubMed] [Google Scholar]
  29. Yau K. W., Baylor D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci. 1989;12:289–327. doi: 10.1146/annurev.ne.12.030189.001445. [DOI] [PubMed] [Google Scholar]
  30. Zhainazarov A. B., Ache B. W. Odor-induced currents in Xenopus olfactory receptor cells measured with perforated-patch recording. J Neurophysiol. 1995 Jul;74(1):479–483. doi: 10.1152/jn.1995.74.1.479. [DOI] [PubMed] [Google Scholar]
  31. Zufall F., Firestein S. Divalent cations block the cyclic nucleotide-gated channel of olfactory receptor neurons. J Neurophysiol. 1993 May;69(5):1758–1768. doi: 10.1152/jn.1993.69.5.1758. [DOI] [PubMed] [Google Scholar]
  32. Zufall F., Shepherd G. M., Firestein S. Inhibition of the olfactory cyclic nucleotide gated ion channel by intracellular calcium. Proc Biol Sci. 1991 Dec 23;246(1317):225–230. doi: 10.1098/rspb.1991.0148. [DOI] [PubMed] [Google Scholar]

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